Journal of
Functional Biomaterials Article
Osseointegration of Titanium Implants in Onlay of Cerament™, a New Ceramic Bone Substitute Anna Truedsson 1, *, Jian-Sheng Wang 2 , Pia Lindberg 1 and Gunnar Warfvinge 1 Received: 21 September 2015; Accepted: 30 December 2015; Published: 7 January 2016 Academic Editor: Adriana Bigi 1 2
*
Department of Oral Pathology, Faculty of Odontology, Malmö University, Malmö SE-205 06, Sweden; [email protected] (P.L.); [email protected] (G.W.) Department of Orthopedics, Lund University Hospital, Lund SE-221 85, Sweden; [email protected] Correspondence: [email protected]; Tel.: +46-40-665-8445; Fax: +46-40-665-8490
Abstract: The purpose was to investigate whether a new biphasic and injectable ceramic bone substitute Cerament™ that rapidly remodels to bone, may contribute to the retention of titanium implant screws during the healing period, and to analyze the pattern of bone formation around titanium implants.Titanium screws were implanted in rat tibiae and embedded with or without Cerament™ on the cortical surface. Torsional resistance was measured after 1 day, and after 6 and 12 weeks. Implant areas without bone substitute were analyzed histologically for comparison. The torsional resistance increased over time as the screws were osseointegrated. There was no difference in resistance between screws embedded in the bone substitute and control screws. The bone apposition was more pronounced on the proximal side of the screw than on the distal side. Cerament™ is capable of conducting bone growth from a cortical bone surface. The newly formed bone in this application does not significantly add to the osseointegrative strength of the implant screw, as measured by torque resistance, during the first 12 weeks. Keywords: animal model; bone substitutes; histological analysis; osseointegration
1. Introduction Dental implants require sufficient retention and often call for augmentation of the alveolar ridge, either as buccal onlays or as augmentation of the floor of the maxillary sinus. Up to now, autologous bone from the jaw or the iliac crest has been the golden standard grafting material when new bone is needed [1,2]. However, a significant drawback of bone grafting is the risk of donor site morbidity [3,4] and in a quest for alternatives, several ceramic bone substitutes have been introduced [5–7]. Biomaterials have thus to some extent reduced the need for bone autografts but as yet, only few have been sufficiently evaluated in order to constitute a reliable option [8]. The outcome measure of bone augmentation is often success of the dental implant in a longer perspective. On the other hand, in experimental settings, retention of implants has been tested with various mechanical tests including pull-out and torque tests. Pull-out tests are more widely used and it has been shown that bone substitutes may add strength to osteoporotic bone [9,10]. Torque tests have been used to investigate if onlay bone grafts may add strength to the integration between bone and dental implants and it has been shown that dental implants anchored to a rabbit cortical bone surface with onlay has a greater removal torque resistance (RTQ) after 24 weeks than control implants without onlay [11,12]. An animal study with various types of grafting material and implants displayed no alteration in torque removal value but differences in bone to implant contact percent [13]. Removal torque is measured in a three-dimensional situation whereas the histological bone to implant contact may be calculated in two dimensions. Many animal studies have been done with different J. Funct. Biomater. 2016, 7, 2; doi:10.3390/jfb7010002
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J. Funct. Biomater. 2016, 7, 2
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J. Funct. Biomater. 2016, 7, 2
implant surface in the purpose to measure correlation between removal torque and bone to implant different implant surface in the purpose to measure correlation between removal torque and bone to contact/bone volume [14–16]. implant contact/bone volume [14–16]. Cerament™ is ais new ceramic bonebone substitute that was designed to treatto spinal Cerament™ a new ceramic substitute that originally was originally designed treat fractures spinal and to fill bone voids. The voids. substitute used in a recent of 33 patients underwent fractures and to fill bone The was substitute was used in study a recent study of 33 who patients who underwent percutaneous after and/or osteoporotic and/or traumatic vertebral Radiological fractures. percutaneous vertebroplastyvertebroplasty after osteoporotic traumatic vertebral fractures. Radiological and clinical outcome was assessed by radiography, CT, and MRI, and 12 months after and clinical outcome was assessed by radiography, CT, and MRI, and 12 months after surgery, the surgery, the fractures new bone formation [17]. mixture It is a biphasic mixture of fractures were stable andwere new stable and bone formation visible [17]. It isvisible a biphasic of calcium sulphate calcium sulphate hemi‐hydrate (CSH) and hydroxyapatite (HA) that has good compressive strength hemi-hydrate (CSH) and hydroxyapatite (HA) that has good compressive strength [18]. CSH is a bone [18]. CSH is a bone substitute with well‐documented ability to support healing in bone defects [19] substitute with well-documented ability to support healing in bone defects [19] but the usefulness but the usefulness of pure CSH in a clinical setting is limited due to its low resistance to resorption of pure CSH in a clinical setting is limited due to its low resistance to resorption [20]. In contrast, [20]. In contrast, hydroxyapatite (HA) has both good mechanical strength and resistance to resorption hydroxyapatite (HA) has both good mechanical strength and resistance to resorption as well as as well as osteoconductive properties [6]. In Cerament™, the CSH component is readily dissolved osteoconductive properties [6]. In Cerament™, the CSH component is readily dissolved leaving HA as leaving HA as a three‐dimensional osteoconductive matrix that allows ingrowth of osteogenic cells a three-dimensional osteoconductive matrix that allows ingrowth of osteogenic cells and vessels. Hence, and vessels. Hence, Cerament™ has many features that are desirable in oral and maxillofacial Cerament™ has many features that are desirable in oral and maxillofacial reconstructive surgery. reconstructive surgery. Experimental evaluation of bone substitutes have primarily been conducted through analysis of Experimental evaluation of bone substitutes have primarily been conducted through analysis of bone ingrowth into drilled defects and other artificial bone voids. Clinically however, the surgeon bone ingrowth into drilled defects and other artificial bone voids. Clinically however, the surgeon is is often with a a need needto toaugment augmentrather ratherthan thanfill filland andthere thereis isa aneed needfor forstudies studies bone often confronted confronted with on on bone substitute onlays. In an experimental onlay model, we have previously shown that Cerament™ may substitute onlays. In an experimental onlay model, we have previously shown that Cerament™ may guide bone toto augment a a cortical detailing histological histologicalfeatures featuresof ofthe the bone guide bone augment cortical bone bone surface surface in in rats, rats, detailing bone remodeling [21]. The purpose of this study was to investigate if Cerament™, and the newly formed remodeling [21]. The purpose of this study was to investigate if Cerament™, and the newly formed bone within it, may also contribute to the retention of implants during the healing period. We have bone within it, may also contribute to the retention of implants during the healing period. We have also histologically studied the bone healing reaction around implants in rat tibia. also histologically studied the bone healing reaction around implants in rat tibia. 2. 2. Results and Discussion Results and Discussion 2.1.2.1. Biomechanical Analysis Biomechanical Analysis The biomechanical testtest waswas performed for all (1 day,(1 6 day, and 12 maximum The biomechanical performed for time all periods time periods 6 weeks). and 12 The weeks). The RTQ increased from 1 day tofrom 6 weeks and toand 12 weeks < 12 0.001; Figure However, maximum RTQ increased 1 day to further 6 weeks further (pto weeks (p
Functional Biomaterials Article
Osseointegration of Titanium Implants in Onlay of Cerament™, a New Ceramic Bone Substitute Anna Truedsson 1, *, Jian-Sheng Wang 2 , Pia Lindberg 1 and Gunnar Warfvinge 1 Received: 21 September 2015; Accepted: 30 December 2015; Published: 7 January 2016 Academic Editor: Adriana Bigi 1 2
*
Department of Oral Pathology, Faculty of Odontology, Malmö University, Malmö SE-205 06, Sweden; [email protected] (P.L.); [email protected] (G.W.) Department of Orthopedics, Lund University Hospital, Lund SE-221 85, Sweden; [email protected] Correspondence: [email protected]; Tel.: +46-40-665-8445; Fax: +46-40-665-8490
Abstract: The purpose was to investigate whether a new biphasic and injectable ceramic bone substitute Cerament™ that rapidly remodels to bone, may contribute to the retention of titanium implant screws during the healing period, and to analyze the pattern of bone formation around titanium implants.Titanium screws were implanted in rat tibiae and embedded with or without Cerament™ on the cortical surface. Torsional resistance was measured after 1 day, and after 6 and 12 weeks. Implant areas without bone substitute were analyzed histologically for comparison. The torsional resistance increased over time as the screws were osseointegrated. There was no difference in resistance between screws embedded in the bone substitute and control screws. The bone apposition was more pronounced on the proximal side of the screw than on the distal side. Cerament™ is capable of conducting bone growth from a cortical bone surface. The newly formed bone in this application does not significantly add to the osseointegrative strength of the implant screw, as measured by torque resistance, during the first 12 weeks. Keywords: animal model; bone substitutes; histological analysis; osseointegration
1. Introduction Dental implants require sufficient retention and often call for augmentation of the alveolar ridge, either as buccal onlays or as augmentation of the floor of the maxillary sinus. Up to now, autologous bone from the jaw or the iliac crest has been the golden standard grafting material when new bone is needed [1,2]. However, a significant drawback of bone grafting is the risk of donor site morbidity [3,4] and in a quest for alternatives, several ceramic bone substitutes have been introduced [5–7]. Biomaterials have thus to some extent reduced the need for bone autografts but as yet, only few have been sufficiently evaluated in order to constitute a reliable option [8]. The outcome measure of bone augmentation is often success of the dental implant in a longer perspective. On the other hand, in experimental settings, retention of implants has been tested with various mechanical tests including pull-out and torque tests. Pull-out tests are more widely used and it has been shown that bone substitutes may add strength to osteoporotic bone [9,10]. Torque tests have been used to investigate if onlay bone grafts may add strength to the integration between bone and dental implants and it has been shown that dental implants anchored to a rabbit cortical bone surface with onlay has a greater removal torque resistance (RTQ) after 24 weeks than control implants without onlay [11,12]. An animal study with various types of grafting material and implants displayed no alteration in torque removal value but differences in bone to implant contact percent [13]. Removal torque is measured in a three-dimensional situation whereas the histological bone to implant contact may be calculated in two dimensions. Many animal studies have been done with different J. Funct. Biomater. 2016, 7, 2; doi:10.3390/jfb7010002
www.mdpi.com/journal/jfb
J. Funct. Biomater. 2016, 7, 2
2 of 9
J. Funct. Biomater. 2016, 7, 2
implant surface in the purpose to measure correlation between removal torque and bone to implant different implant surface in the purpose to measure correlation between removal torque and bone to contact/bone volume [14–16]. implant contact/bone volume [14–16]. Cerament™ is ais new ceramic bonebone substitute that was designed to treatto spinal Cerament™ a new ceramic substitute that originally was originally designed treat fractures spinal and to fill bone voids. The voids. substitute used in a recent of 33 patients underwent fractures and to fill bone The was substitute was used in study a recent study of 33 who patients who underwent percutaneous after and/or osteoporotic and/or traumatic vertebral Radiological fractures. percutaneous vertebroplastyvertebroplasty after osteoporotic traumatic vertebral fractures. Radiological and clinical outcome was assessed by radiography, CT, and MRI, and 12 months after and clinical outcome was assessed by radiography, CT, and MRI, and 12 months after surgery, the surgery, the fractures new bone formation [17]. mixture It is a biphasic mixture of fractures were stable andwere new stable and bone formation visible [17]. It isvisible a biphasic of calcium sulphate calcium sulphate hemi‐hydrate (CSH) and hydroxyapatite (HA) that has good compressive strength hemi-hydrate (CSH) and hydroxyapatite (HA) that has good compressive strength [18]. CSH is a bone [18]. CSH is a bone substitute with well‐documented ability to support healing in bone defects [19] substitute with well-documented ability to support healing in bone defects [19] but the usefulness but the usefulness of pure CSH in a clinical setting is limited due to its low resistance to resorption of pure CSH in a clinical setting is limited due to its low resistance to resorption [20]. In contrast, [20]. In contrast, hydroxyapatite (HA) has both good mechanical strength and resistance to resorption hydroxyapatite (HA) has both good mechanical strength and resistance to resorption as well as as well as osteoconductive properties [6]. In Cerament™, the CSH component is readily dissolved osteoconductive properties [6]. In Cerament™, the CSH component is readily dissolved leaving HA as leaving HA as a three‐dimensional osteoconductive matrix that allows ingrowth of osteogenic cells a three-dimensional osteoconductive matrix that allows ingrowth of osteogenic cells and vessels. Hence, and vessels. Hence, Cerament™ has many features that are desirable in oral and maxillofacial Cerament™ has many features that are desirable in oral and maxillofacial reconstructive surgery. reconstructive surgery. Experimental evaluation of bone substitutes have primarily been conducted through analysis of Experimental evaluation of bone substitutes have primarily been conducted through analysis of bone ingrowth into drilled defects and other artificial bone voids. Clinically however, the surgeon bone ingrowth into drilled defects and other artificial bone voids. Clinically however, the surgeon is is often with a a need needto toaugment augmentrather ratherthan thanfill filland andthere thereis isa aneed needfor forstudies studies bone often confronted confronted with on on bone substitute onlays. In an experimental onlay model, we have previously shown that Cerament™ may substitute onlays. In an experimental onlay model, we have previously shown that Cerament™ may guide bone toto augment a a cortical detailing histological histologicalfeatures featuresof ofthe the bone guide bone augment cortical bone bone surface surface in in rats, rats, detailing bone remodeling [21]. The purpose of this study was to investigate if Cerament™, and the newly formed remodeling [21]. The purpose of this study was to investigate if Cerament™, and the newly formed bone within it, may also contribute to the retention of implants during the healing period. We have bone within it, may also contribute to the retention of implants during the healing period. We have also histologically studied the bone healing reaction around implants in rat tibia. also histologically studied the bone healing reaction around implants in rat tibia. 2. 2. Results and Discussion Results and Discussion 2.1.2.1. Biomechanical Analysis Biomechanical Analysis The biomechanical testtest waswas performed for all (1 day,(1 6 day, and 12 maximum The biomechanical performed for time all periods time periods 6 weeks). and 12 The weeks). The RTQ increased from 1 day tofrom 6 weeks and toand 12 weeks < 12 0.001; Figure However, maximum RTQ increased 1 day to further 6 weeks further (pto weeks (p
